, Volume 15, Issue 8, pp 1271–1282 | Cite as

Grass Invasions Across a Regional Gradient are Associated with Declines in Belowground Carbon Pools

  • Timothy D. Kramer
  • Robert J. WarrenII
  • Yaya Tang
  • Mark A. Bradford


The composition of plant communities everywhere now likely comprises alien as well as native species, and those aliens that become invasive have wide-ranging impacts on the structure and function of recipient ecosystems. These impacts include perturbations to soil carbon (C) cycling, but the direction and magnitude of impacts are species and climate dependent, making it difficult to generalize whether a specific invader will promote losses or gains in soil C stocks. Generalizations of a specific invader’s impacts are necessary; however, because the range of an invader can encompass thousands of square kilometers, meaning their effects can have broad, regional consequences. To quantify broad-scale and context-dependent impacts of a specific invader, multi-site investigations that capture and measure local and regional environmental heterogeneity are necessary. Using this approach, we show that a widespread grass invader of forest understories is associated with declines in soil C during infilling (spreading within the invaded range). Across the 36 study sites, total soil C stocks declined (P = 0.113) by approximately 12% (estimated mean ± SD, uninvaded: 2,429 ± 512.9 vs. invaded: 2,140 ± 520.7 g C m−2). The decline in total soil C is driven by a significant (P = 0.047) reduction in the native-derived, mineral-associated soil C fraction. This fraction, whose mass and slow turnover makes it an important C store, is approximately 15% lower in invaded (estimated mean ± SD: 1,560 ± 400.4 g C m−2) than uninvaded plots (1,826 ± 398.1 g C m−2). Notably, declines in this C fraction are only apparent at 21 of the sites, reflecting how environmental heterogeneity in other variables (specifically pH, soil moisture, and clay content) are important to quantify to determine invader impacts across a region. The 26% decline in microbial biomass with invasion (P = 0.011; estimated mean ± SD, uninvaded: 10.05 ± 1.79 vs. invaded: 7.40 ± 1.80 g C m−2) is also dependent on site characteristics (pH), and reductions are greater where the invader occurs at higher densities. Reductions in microbial biomass and soil C with invasion suggest that grass invasion will alter soil C cycling and decrease forest-C stores across the study region, although invader effects at a specific-site will be dependent on environmental context.


soil organic matter soil carbon storage carbon cycling microbial biomass exotic species alien species Microstegium vimineum linear mixed models environmental heterogeneity context dependency 

Supplementary material

10021_2012_9583_MOESM1_ESM.doc (480 kb)
Supplementary material 1 (DOC 479 kb)


  1. Anderson JPE, Domsch KH. 1978. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–21.Google Scholar
  2. Baath E, Nerg B, Lohm U, Lundgren B, Lundkvist H, Rosswall T, Soderstrom B, Wiren A. 1980. Effects of experimental acidification and liming on soil organisms and decomposition in a Scots pine forest. Pedobiologia 20:85–100.Google Scholar
  3. Baayen RH. 2007. Analyzing linguistic data: a practical introduction to statistics using R. Cambridge: Cambridge University Press.Google Scholar
  4. Blumenthal D. 2006. Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–95.PubMedCrossRefGoogle Scholar
  5. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, White JS. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–35.PubMedCrossRefGoogle Scholar
  6. Bradford MA, Fierer N, Reynolds JF. 2008. Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils. Funct Ecol 22:964–74.CrossRefGoogle Scholar
  7. Bradford MA, Strickland MS, DeVore JL, Maerz JC. 2012. Root carbon flow from an invasive plant to belowground foodwebs. Plant Soil . doi:10.1007/s11104-012-1210-y.Google Scholar
  8. Bradley BA, Houghton RA, Mustard JF, Hamburg SP. 2006. Invasive grass reduces aboveground carbon stocks in shrublands of the Western US. Glob Change Biol 12:1815–22.CrossRefGoogle Scholar
  9. Carney KM, Hungate BA, Drake BG, Megonigal JP. 2007. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci USA 104:4990–5.PubMedCrossRefGoogle Scholar
  10. Chatterjee S, Hadi AS, Price B. 2000. Regression analysis by example. New York: Wiley.Google Scholar
  11. Cole PG, Weltzin JF. 2004. Environmental correlates of the distribution and abundance of Microstegium vimineum, in east Tennessee. Southeast Nat 3:545–62.CrossRefGoogle Scholar
  12. Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins F, Hyvönen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Steinweg JM, Wallenstein MD, Wetterstedt JÅM, Bradford MA. 2011. Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Glob Change Biol 17:3392–404.CrossRefGoogle Scholar
  13. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–73.PubMedCrossRefGoogle Scholar
  14. Ehrenfeld JG. 2003. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–23.CrossRefGoogle Scholar
  15. Ehrenfeld JG, Kourtev P, Huang WZ. 2001. Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–300.CrossRefGoogle Scholar
  16. Engqvist L. 2005. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–71.CrossRefGoogle Scholar
  17. Fairbrothers DE, Gray JR. 1972. Microstegium vimineum (Trin) A. Camus (Gramineae) in the United-States. Bull Torrey Bot Club 99:97–100.CrossRefGoogle Scholar
  18. Fierer N, Schimel JP, Holden PA. 2003. Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–76.CrossRefGoogle Scholar
  19. Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC. 2009. Global patterns in belowground communities. Ecol Lett 12:1238–49.PubMedCrossRefGoogle Scholar
  20. Flory SL, Clay K. 2009a. Invasive plant removal method determines native plant community responses. J Appl Ecol 46:434–42.CrossRefGoogle Scholar
  21. Flory SL, Clay K. 2009b. Non-native grass invasion alters native plant composition in experimental communities. Biol Invasions 12:1285–94.CrossRefGoogle Scholar
  22. Gee GW, Or D. 2002. Particle-size analysis. In: Dane JH, Topp GC, Eds. Methods of soil analysis, Part 4: Physical methods. Madison, WI: Soil Science Society of America. Google Scholar
  23. Grandy AS, Neff JC. 2008. Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307.PubMedCrossRefGoogle Scholar
  24. Hurlbert SH, Lomabardi CM. 2009. Final collapse of the Neyman–Pearson decision theoretic framework and rise of the neoFisherian. Ann Zool Fenn 46:311–49.CrossRefGoogle Scholar
  25. Ineson P, Cotrufo MF, Bol R, Harkness DD, Blum H. 1996. Quantification of soil carbon inputs under elevated CO2:C-3 plants in a C-4 soil. Plant Soil 187:345–50.CrossRefGoogle Scholar
  26. Jackson RB, Banner JL, Jobbágy EG, Pockman WT, Wall DH. 2002. Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418:623–6.PubMedCrossRefGoogle Scholar
  27. Kourtev PS, Ehrenfeld JG, Huang WZ. 1998. Effects of exotic plant species on soil properties in hardwood forests of New Jersey. Water Air Soil Pollut 105:493–501.CrossRefGoogle Scholar
  28. Kourtev PS, Ehrenfeld JG, Huang WZ. 2002. Enzyme activities during litter decomposition of two exotic and two native plant species in hardwood forests of New Jersey. Soil Biol Biochem 34:1207–18.CrossRefGoogle Scholar
  29. Kuzyakov Y. 2010. Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–71.CrossRefGoogle Scholar
  30. Lal R. 2004. Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–7.PubMedCrossRefGoogle Scholar
  31. Liao C, Peng R, Luo YQ, Zhou X, Wu X, Fang C, Chen J, Li B. 2008. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–14.PubMedCrossRefGoogle Scholar
  32. Litton CM, Sanquist DR, Cordell S. 2008. A non-native invasive grass increases soil carbon flux in a Hawaiian tropical dry forest. Glob Change Biol 14:726–39.CrossRefGoogle Scholar
  33. Liu F, Wu B, Bai E, Boutton TW, Archer SR. 2011. Quantifying soil organic carbon in complex landscapes: an example of grassland undergoing encroachment of woody plants. Glob Change Biol 17:1119–29.CrossRefGoogle Scholar
  34. MacDougall AS, Boucher J, Turkington R, Bradfield GE. 2006. Patterns of plant invasion along an environmental stress gradient. J Veg Sci 17:47–56.CrossRefGoogle Scholar
  35. Mack M, D’Antonio CM. 2003. The effects of exotic grasses on litter decomposition in a Hawaiian woodland—the importance of indirect effects. Ecosystems 6:723–38.CrossRefGoogle Scholar
  36. Maindonald JH, Braun J. 2003. Data analysis and graphics using R: an example-based approach. Cambridge: Cambridge University Press.Google Scholar
  37. Martin PH, Canham CD, Marks PL. 2009. Why forests appear resistant to exotic plant invasions: intentional introductions, stand dynamics, and the role of shade tolerance. Front Ecol Environ 7:142–9.CrossRefGoogle Scholar
  38. Muirhead JR, Leung B, van Overdijk C, Kelly DW, Nandakumar K, Marchant KR, MacIsaac HJ. 2006. Modelling local and long-distance dispersal of invasive emerald ash borer Agrilus planipennis (Coleoptera) in North America. Diversity Distrib 12:71–9.CrossRefGoogle Scholar
  39. Oswalt CM, Oswalt SN, Clatterbuck WK. 2007. Effects of Microstegium Vimineum (Trin.) A. Camus on native woody species density and diversity in a productive mixed-hardwood forest in Tennessee. For Ecol Manage 242:727–32.CrossRefGoogle Scholar
  40. R Development Core Team. 2009. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  41. Saby NPA, Arrouays D, Antoni V, Lemercier B, Follain S, Walter C, Schvartz C. 2008. Changes in soil organic carbon in a mountainous French region, 1990–2004. Soil Use Manag 24:254–62.CrossRefGoogle Scholar
  42. Schimel DS, Braswell BH, Holland EA, McKeown R, Ojima DS, Painter TH, Parton WJ, Townsend AR. 1994. Climatic, edaphic, and biotic controls over storage and turnover of carbon in soils. Glob Biogeochem Cycles 8:279–93.CrossRefGoogle Scholar
  43. Schlesinger WH, Lichter J. 2001. Limited carbon storage in soil and litter of experimental forest plots under increased CO2. Nature 411:466–9.PubMedCrossRefGoogle Scholar
  44. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478:49–56.PubMedCrossRefGoogle Scholar
  45. Sollins P, Glassman C, Paul EA, Swanston C, Lajtha K, Heil JW, Elliott ET. 1999. Soil carbon and nitrogen. Pools and fractions. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P, Eds. Standard soil methods for long-term ecological research. New York: Oxford University Press. p 89–105.Google Scholar
  46. Staddon PL. 2004. Carbon isotopes in functional soil ecology. Trends Ecol Evol 19:148–54.PubMedCrossRefGoogle Scholar
  47. Strickland MS, DeVore JL, Maerz JC, Bradford MA. 2010. Grass invasion of a hardwood forest is associated with declines in belowground carbon pools. Glob Change Biol 16:1338–50.CrossRefGoogle Scholar
  48. Strickland MS, DeVore JL, Maerz JC, Bradford MA. 2011. Loss of faster-cycling soil carbon pools following grass invasion across multiple forest sites. Soil Biol Biochem 43:452–4.CrossRefGoogle Scholar
  49. Throop HL, Archer SR. 2008. Shrub (Prosopis velutina) encroachment in a semidesert grassland: spatial–temporal changes in soil organic carbon and nitrogen pools. Glob Change Biol 14:2420–31.CrossRefGoogle Scholar
  50. Václavík T, Meentemeyer RK. 2012. Equilibrium or not? Modelling potential distribution of invasive species in different stages of invasion. Diversity Distrib 18:73–83.CrossRefGoogle Scholar
  51. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P. 2011. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–8.PubMedCrossRefGoogle Scholar
  52. Warren RJ, Bradford MA. 2011. The shape of things to come: woodland herb niche contraction begins during recruitment in mesic forest microhabitat. Proc R Soc Lond B 278:1390–8.CrossRefGoogle Scholar
  53. Warren RJ, Bahn V, Kramer TD, Tang Y, Bradford MA. 2011a. Performance and reproduction of an exotic invader across temperate forest gradients. Ecosphere 2:14.CrossRefGoogle Scholar
  54. Warren RJ, Wright JP, Bradford MA. 2011b. The putative niche requirements and landscape dynamics of Microstegium vimineum: an invasive Asian grass. Biol Invasions 13:471–83.CrossRefGoogle Scholar
  55. Wolkovich EM, Lipson DA, Virginia RA, Cottingham KL, Bolger DT. 2010. Grass invasion causes rapid increases in ecosystem carbon and nitrogen storage in a semiarid shrubland. Glob Change Biol 16:1351–65.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Timothy D. Kramer
    • 1
  • Robert J. WarrenII
    • 1
  • Yaya Tang
    • 1
  • Mark A. Bradford
    • 1
  1. 1.School of Forestry and Environmental StudiesYale UniversityNew HavenUSA

Personalised recommendations